Biochemical characterization of the respiratory syncytial virus N0-P complex in solution

J Biol Chem. 2019 Mar 8;294(10):3647-3660. doi: 10.1074/jbc.RA118.006453. Epub 2019 Jan 9.

Abstract

As all the viruses belonging to the Mononegavirales order, the nonsegmented negative-strand RNA genome of respiratory syncytial virus (RSV) is encapsidated by the viral nucleoprotein N. N protein polymerizes along the genomic and anti-genomic RNAs during replication. This requires the maintenance of the neosynthesized N protein in a monomeric and RNA-free form by the viral phosphoprotein P that plays the role of a chaperone protein, forming a soluble N0-P complex. We have previously demonstrated that residues 1-30 of P specifically bind to N0 Here, to isolate a stable N0-P complex suitable for structural studies, we used the N-terminal peptide of P (P40) to purify truncated forms of the N protein. We show that to purify a stable N0-P-like complex, a deletion of the first 30 N-terminal residues of N (NΔ30) is required to impair N oligomerization, whereas the presence of a full-length C-arm of N is required to inhibit RNA binding. We generated structural models of the RSV N0-P with biophysical approaches, including hydrodynamic measurements and small-angle X-ray scattering (SAXS), coupled with biochemical and functional analyses of human RSV (hRSV) NΔ30 mutants. These models suggest a strong structural homology between the hRSV and the human metapneumovirus (hMPV) N0-P complexes. In both complexes, the P40-binding sites on N0 appear to be similar, and the C-arm of N provides a high flexibility and a propensity to interact with the N RNA groove. These findings reveal two potential sites to target on N0-P for the development of RSV antivirals.

Keywords: N0-P complex; analytical ultracentrifugation; mutagenesis; nucleoprotein N; protein folding; respiratory syncytial virus; small-angle X-ray scattering (SAXS); structural model; structure-function; viral replication.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Binding Sites
  • DNA-Directed RNA Polymerases / genetics
  • DNA-Directed RNA Polymerases / metabolism
  • Models, Molecular
  • Mutation
  • Nucleoproteins / chemistry*
  • Nucleoproteins / genetics
  • Nucleoproteins / metabolism*
  • Protein Conformation
  • Respiratory Syncytial Virus, Human*
  • Solutions
  • Surface Properties
  • Viral Proteins / chemistry*
  • Viral Proteins / genetics
  • Viral Proteins / metabolism*

Substances

  • Nucleoproteins
  • Solutions
  • Viral Proteins
  • DNA-Directed RNA Polymerases

Associated data

  • PDB/2WJ8
  • PDB/5FVD